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(E)-Β-Caryophyllene: a Systematic Quantitative Analysis of Published Literature

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(E)-Β-Caryophyllene: a Systematic Quantitative Analysis of Published Literature International Journal of Molecular Sciences Article Plant Natural Sources of the Endocannabinoid (E)-β-Caryophyllene: A Systematic Quantitative Analysis of Published Literature Massimo E. Maffei y Department of Life Sciences and Systems Biology, University of Turin, Via Quarello 15/a, 10135 Turin, Italy; massimo.maff[email protected]; Tel.: +39-011-670-5967 This work is dedicated to Husnu Can Baser for his 70th birthday. y Received: 7 August 2020; Accepted: 4 September 2020; Published: 7 September 2020 Abstract: (E)-β-caryophyllene (BCP) is a natural sesquiterpene hydrocarbon present in hundreds of plant species. BCP possesses several important pharmacological activities, ranging from pain treatment to neurological and metabolic disorders. These are mainly due to its ability to interact with the cannabinoid receptor 2 (CB2) and the complete lack of interaction with the brain CB1. A systematic analysis of plant species with essential oils containing a BCP percentage > 10% provided almost 300 entries with species belonging to 51 families. The essential oils were found to be extracted from 13 plant parts and samples originated from 56 countries worldwide. Statistical analyses included the evaluation of variability in BCP% and yield% as well as the statistical linkage between families, plant parts and countries of origin by cluster analysis. Identified species were also grouped according to their presence in the Belfrit list. The survey evidences the importance of essential oil yield evaluation in support of the chemical analysis. The results provide a comprehensive picture of the species with the highest BCP and yield percentages. Keywords: plant species; essential oil; yield; percentages of (E)-β-caryophyllene; Belfrit list; plant part; geographical origin 1. Introduction The endogenous cannabinoid system (ECS) plays an important role in the immune response to an infection. At present, two cannabinoid (CB) receptors are described: cannabinoid type 1 receptor (CB1) and cannabinoid type 2 receptor (CB2), both G-protein coupled receptors [1]. The CB2 receptor represents the peripheral CB, due to its expression on circulating immune cells. However, studies have also found CB2 expression in the brain, such as cerebellum and microglial cells [2]. The CB2 receptor is involved in the attenuation of inflammatory immune responses. CB2 receptor pathway activation entails the suppression of cytokine release from immune cells and thereby dampening of the inflammatory response (immunosuppression) [3]. (E)-β-caryophyllene (BCP) is a bicyclic sesquiterpene hydrocarbon which is present in the essential oil of several plant species [4]. The Research Institute for Fragrance Materials (RIFM) evaluated BCP safety and the molecule has been approved by the Food and Drug Administration and by the European Food Safety Authority as a flavoring agent, which can be used in cosmetic and food additives [5]. Reports on oral sub-chronic toxicity support the safety of BCP for its proposed use also in medical food products [5]. BCP has been reported to be active against several disorders, with particular reference to cancer, chronic pain and inflammation [2]. Non-clinical BCP toxicity and an absence of adverse effects have been described [6]. Moreover, BCP can act as a selective agonist of CB2 [1], it activates peroxisome proliferator-activated receptor-α (PPAR α)[7] and has been recently involved in the prevention of Int. J. Mol. Sci. 2020, 21, 6540; doi:10.3390/ijms21186540 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 6540 2 of 37 lipid accumulation and in the improvement of glucose uptake [8]. Therefore, BCP is a plant-derived bioactive molecule able to improve health and prevent lifestyle diseases. Moreover, the specificity of BCP for the CB2 receptor, mainly expressed in peripheral tissues, and its inability to bind CB1, which is predominantly expressed at the level of the central nervous system, implies that its action is devoid of the known psychoactive effects associated with the activation of CB1 [1,2,9,10]. In this context, BCP is an interesting alternative to the use of Cannabis. Owing to the growing importance of BCP, it was interesting to evaluate the occurrence of this important endocannabinoid in plant species used for the extraction of essential oils. Therefore, the aim of this work was to look for plant natural sources of BCP in order to provide the pharmaceutical, nutraceutical and aroma industries a summary of plant species, parts used for extraction and geographical origin of plants producing BCP. Moreover, additional information was provided with regards to the content and yield of BCP as well as the occurrence of selected species in the Belfrit list [11], which includes botanicals allowed in food supplements and ensures compliance of botanicals in terms of quality and safety. 2. Results and Discussion The database search (performed in July 2020) for the term caryophyllene provided 5867 entries. The search was then refined by selecting all papers with a chemical composition description. This selection provided 2604 entries, which were individually analyzed in order to select papers providing information on BCP percentage > 10%. Papers were then analyzed and the species binomial name, the plant family, the country of origin of samples and the plant part extracted were reported along with the BCP percentage and yield percentage. The total number of selected species was 295 (Table1). Table1 also lists the presence of the species in the Belfrit list [11]. In general, the 295 species belonged to 51 families and were reported from 56 countries worldwide. The essential oil containing BCP was extracted from 13 different plant parts. Out of 295 species, 34 were found to be listed in the Belfrit list, whereas for 51 species no data were available on the yield percentage. In many cases, the researchers used a small amount of plant parts (ranging from a few g to 200–300 g) from which it was impossible to evaluate the oil yield. However, in the majority of the other cases the yield was provided and hence reported (Table1). Int. J. Mol. Sci. 2020, 21, 6540 3 of 37 Table1. Occurrence of (E)-β-caryophyllene (BCP) in different plant species. n.a., data not available, the essential oil (E.O.) yield is expressed as volume/weight percentage. Family Genus Species and Auth Geogr. Origin of Sample Belfrit List Part Used E.O. Yield% BCP% Code Ref. Anacardiaceae Rhus coriaria L. Iran YES fruits 0.55 34.3 249 [12] Anacardiaceae Spondias pinnata (Linn. F.) Kurz Egypt NO leaves 2.00 49.9 268 [13] Annonaceae Annona muricata L. Bénin YES leaves 0.10 13.6 30 [14] Annonaceae Annona densicoma Mart. Brazil NO leaves 0.10 14.4 31 [15] Annonaceae Annona senegalensis Pers. Burkina Faso NO leaves 0.73 19.1 32 [16] Annonaceae Annona squamosa L. India YES leaves 0.12 22.9 33 [17] Annonaceae Artabotrys hexapetalus (L. f.) Bhandare Vietnam NO flowers 0.94 11.4 38 [18] odorata (Lam.) Hook.f. and Annonaceae Cananga Australia YES leaves 0.30 52.0 62 [19] Thomson glauca Pierre ex Engler and Annonaceae Cleistopholis Ivory Coast NO leaves 0.19 26.2 81 [20] Diels Annonaceae Fissistigma rubiginosum Merr. Vietnam NO leaves 0.30 28.1 125 [21] Annonaceae Goniothalamus multiovulatus Ast Vietnam NO stems 0.21 35.7 135 [22] sp. (Dunal) Hook.f. and Annonaceae Melodorum Australia NO leaf 0.15 26.7 182 [23] Thomson horsfieldii (Bennett) Baillon ex Annonaceae Miliusa Australia NO leaves 0.1 20.2 188 [24] Pierre Annonaceae Mitrephora zippeliana Miq. Australia NO leaves 0.30 18.1 189 [19] Annonaceae Polyalthia oliveri Engl. Ivory Coast NO leaves 0.13 31.4 237 [25] Annonaceae Pseuduvaria hylandii Jessup Australia NO leaves 0.50 24.1 242 [26] Annonaceae Uvariodendron calophyllum R. E. Fries Cameroon NO stem barks 0.52 32.5 284 [27] erecta (Hudson) Coville subsp. Apiaceae Berula Serbia NO aerial parts 0.01 14.9 52 [28] erecta Apiaceae Bilacunaria anatolica A. Duran Turkey NO aerial parts 0.14 10.3 54 [29] Apiaceae Centella asiatica L. South Africa YES aerial parts 0.06 19.1 75 [30] Apiaceae Conium maculatum L. Iran NO aerial parts 0.20 15.3 85 [31] Apiaceae Dorema aucheri Boiss. Iran NO leaves 0.40 35.7 108 [32] Apiaceae Eryngium vesiculosum Labill. Australia NO aerial parts n.a. 20.3 116 [33] Apiaceae Ferula glauca L. Iran NO leaves 0.07 24.9 123 [34] Int. J. Mol. Sci. 2020, 21, 6540 4 of 37 Table 1. Cont. Family Genus Species and Auth Geogr. Origin of Sample Belfrit List Part Used E.O. Yield% BCP% Code Ref. Apiaceae Grammosciadium pterocarpum Boiss. Turkey NO aerial parts n.a. 15.3 136 [35] microcarpum (M. Bieb.) B. Apiaceae Hippomarathrum Iran NO aerial parts 0.85 15.75 145 [36] Fedtsch Apiaceae Hippomarathrum boissieri Reuter et Hausskn Turkey NO aerial parts 0.40 25.6 146 [37] Apiaceae Laser trilobum (L.) Borkh. Iran NO aerial parts 1.80 22.4 165 [38] Apiaceae Oenanthe divaricata (R. Br.) Mabb. Spain NO aerial parts 0.20 15.3 206 [39] viridiflorum (Turcz.) Apiaceae Ostericum China NO aerial parts 0.03 24.3 210 [40] Kitagawa Apiaceae Pimpinella kotschyana Boiss. Iran NO seeds 5.16 49.9 224 [41] Apiaceae Prangos uloptera DC. Iran NO aerial parts 0.70 18.2 240 [42] Apiaceae Zosima absinthifolia Link Iran NO aerial parts 0.20 22.2 295 [43] Apocynaceae Allamanda cathartica L. Brazil NO flowers n.a. 15.7 21 [44] Apocynaceae Aspidosperma cylindrocarpon Muell. Arg. Brazil NO leaves 0.03 14.3 45 [45] Apocynaceae Tabernaemontana catharinensis A. DC. Brazil NO leaves 0.30 56.9 272 [46] Araliaceae Schefflera stellata (Gaertn.) Harms India NO leaves 0.10 19.2 260 [47] Aristolochiaceae Aristolochia elegans Mast. Argentina NO leaves n.a. 27.8 36 [48] Aristolochiaceae Aristolochia fordiana Hemsl China NO aerial parts 0.19 11.1 37 [49] Asteraceae Achillea asplenifolia Vent.
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